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While playing in a bar in St. Louis, jazz pianist Jigger Pine meets aspiring clarinetist Nickie Haroyen who tries to convince him to put together a jazz band. After a drunk patron starts a fight, Nickie and Jigger are thrown in jail with Jigger's drummer and bassist. They hear a prisoner singing a blues song and are inspired to set out for New Orleans where they hope to learn how to perfect an authentic bluesy sound. There they meet fast-talking trumpeter Leo and his wife Character who is a talented singer. Together, the quintet rides the rails, honing their technique in dive bars across the country.

One day while sheltering in a boxcar they meet a mysterious stranger named Del, who robs them. But when they don't turn him in to the authorities, Del, impressed by their camaraderie, offers them a job in a New Jersey roadhouse called The Jungle. The group discovers that the roadhouse is actually owned by Del's former partners in crime, aspiring singer Kay, accomplice Sam and her crippled sidekick Brad. Del has escaped from jail to retrieve his share of a robbery the three committed, but when Kay tells him they have spent all the money, he decides to take over The Jungle and transform it into an illegal gambling club. Kay tries to rekindle her past romance with Del, but he rejects her and she turns her attention to Leo in hopes of making Del jealous. Although the band is happy playing their brand of jazz each night at the club, Character is worried about Leo and Kay. Jigger reveals to Leo that Character is pregnant and he decides to give up Kay. She soon sets her sights on Jigger, who is secretly in love with her. When Sam tries to get her to alert the police to Del's whereabouts, she tells Del, hoping to win him back. Sam is killed by Del's henchmen, and Del orders Kay to leave The Jungle. She convinces Jigger to quit the band and go with her to New York City to join a more commercial, mainstream jazz band.

Although successful, Jigger is unhappy in his new life, feeling he is not playing authentic jazz. Kay eventually grows bored of life with Jigger and leaves him when he tells her he is quitting the band. He descends into alcoholism and has a mental breakdown. His friends find him and help nurse him back to health, hiding the fact that Character's baby has died. They return to The Jungle where Jigger begins playing again. Soon afterward, Kay shows up without any money, begging Del to take her back. He refuses, she threatens to turn him in, and he pulls a gun on her. Jigger comes to her defense and in the ensuing fight, when Del drops his gun, Kay picks it up and shoots and kills him. Jigger decides to protect Kay and help her escape from the police, but Brad hears their plans and realizes that Kay is leaving forever. The band shows up and try to talk Jigger out of leaving with Kay, revealing that Character lost the baby. They compare Jigger's mental problems with Brad being a cripple, stating that Brad has no choice about how he will end up but Jigger does have a choice. Brad overhears the band. He joins Kay in Del's car where she has been waiting for Jigger. Brad drives away with her into a violent storm, deliberately wrecking the car and killing them both. The band resolves to leave The Jungle behind and they return to their life on the road, happy to be playing their preferred version of jazz again.

The film began when Elia Kazan optioned an unproduced play by Edwin Gilbert called Hot Nocturne and began retooling it for Broadway. He eventually sold the rights to Warner Bros. who gave the script to Robert Rossen to complete. After initially retitling it New Orleans Blues, the studio named it after its principal musical number "Blues in the Night", which later became a popular hit. Kazan agreed to give up his screenwriting credit and appeared as a clarinetist in the film. He later remarked that after acting in the film he became convinced he could "direct better than Anatole Litzvak".[3]James Cagney and Dennis Morgan were the studio's first two choices to play the gangster Del Davis, but the role was eventually given to Lloyd Nolan. John Garfield was cast in the role of pianist Jigger Pine who was eventually played by Richard Whorf.[4]

The film's music is by Harold Arlen with lyrics by Johnny Mercer. Additional music was written by Heinz Roemheld and Ray Heindorf (only Roemheld was credited). The film features the bands of Jimmie Lunceford and Will Osborne. With the exception of Priscilla Lane none of the actors were musicians so their playing had to be dubbed by other artists. The trumpet music performed by Jack Carson's character was dubbed by Snooky Young and Frankie Zinzer while the piano music was dubbed by Stan Wrightsman.[2][5] Saxophonist and clarinetist Archie Rosate played Elia Kazan's clarinet solos.

Blues in the Night was met with a mixed critical reception upon its release. Hollywood columnist Fred Othman named it "the worst musical of the year".[7] Donald Kirkley of The Baltimore Sun called it "a bizarre...screen oddity"[8] while Los Angeles Times film critic Philip K. Scheuer praised Richard Whorf's performance.[9] It was not financially successful as its East Coast release took place shortly before the attack on Pearl Harbor.